Septohippocampal Neuromodulation Improves Cognition after Traumatic Brain Injury

Journal of Neurotrauma

Volumn 32, Issue 22, 2015, Pages 1822-1832

  Lee, Darrin J ^a   Gurkoff, Gene G ^a   Izadi, Ali ^a   Seidl, Stacey E ^a   Echeverri, Angela ^a   Melnik, Mikhail ^a   Berman, Robert F ^a,b   Ekstrom, Arne D ^b   Muizelaar, J Paul ^a   Lyeth, Bruce G ^a,b   Shahlaie, Kiarash ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cognition; deep brain stimulation; hippocampal theta oscillation; medial septal nucleus; traumatic brain injury

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BARNES MAZE TEST; BRAIN DEPTH STIMULATION; COGNITIVE DEFECT; CONTROLLED STUDY; DEPTH ELECTRODE; ELECTRODE IMPLANTATION; EXPLORATORY BEHAVIOR; GAMMA RHYTHM; HIPPOCAMPUS; IPSILATERAL HIPPOCAMPUS; MALE; MEDIAL SEPTAL NUCLEUS; NONHUMAN; OSCILLATION; POSTTRAUMATIC COMPLICATION; RAT; SEPTUM NUCLEUS; SPATIAL LEARNING; THETA RHYTHM; TRAUMATIC BRAIN INJURY; TREATMENT OUTCOME; ANIMAL; BRAIN INJURY; COGNITION DISORDERS; ELECTRODE IMPLANT; ELECTROENCEPHALOGRAPHY; ELECTROTHERAPY; MAZE TEST; PATHOPHYSIOLOGY; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN INJURIES; COGNITION DISORDERS; ELECTRIC STIMULATION THERAPY; ELECTRODES, IMPLANTED; ELECTROENCEPHALOGRAPHY; EXPLORATORY BEHAVIOR; GAMMA RHYTHM; HIPPOCAMPUS; MALE; MAZE LEARNING; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; SEPTAL NUCLEI; THETA RHYTHM;

EID: 84947079103     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2014.3744     Document Type: Article

References (73)

1. Slovarp, L., Azuma, T., and Lapointe, L. (2012). The effect of traumatic brain injury on sustained attention and working memory. Brain Inj. 26, 48-57.
2. Palacios, E.M., Sala-Llonch, R., Junque, C., Roig, T., Tormos, J.M., Bargallo, N., and Vendrell, P. (2012). White matter integrity related to functional working memory networks in traumatic brain injury. Neurology 78, 852-860.
3. Laxton, A.W., Tang-Wai, D.F., McAndrews, M.P., Zumsteg, D., Wennberg, R., Keren, R., Wherrett, J., Naglie, G., Hamani, C., Smith, G.S., and Lozano, A.M. (2010). A phase I trial of deep brain stimulation of memory circuits in Alzheimer's disease. Ann Neurol. 68, 521-534.
4. Suthana, N., Haneef, Z., Stern, J., Mukamel, R., Behnke, E., Knowlton, B., and Fried, I. (2012). Memory enhancement and deep-brain stimulation of the entorhinal area. N. Engl. J. Med. 366, 502-510.
5. Vertes, R.P. (2005). Hippocampal theta rhythm: a tag for short-term memory. Hippocampus 15, 923-935.
6. Winson, J. (1978). Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201, 160-163.
7. Buzsaki, G. (2005). Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827-840.
8. McNaughton, N., Ruan, M., and Woodnorth, M.A. (2006). Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16, 1102-1110.
9. Mizumori, S.J., Barnes, C.A., and McNaughton, B.L. (1990). Behavioral correlates of theta-on and theta-off cells recorded from hippocampal formation of mature young and aged rats. Exper. Brain Res. 80, 365-373.
10. Cashdollar, N., Malecki, U., Rugg-Gunn, F.J., Duncan, J.S., Lavie, N., and Duzel, E. (2009). Hippocampus-dependent and -independent thetanetworks of active maintenance. Proc. Natl. Acad. Sci. U. S. A.106, 20493-20498.
11. Ekstrom, A.D., Caplan, J.B., Ho, E., Shattuck, K., Fried, I., and Kahana, M.J. (2005). Human hippocampal theta activity during virtual navigation. Hippocampus, 15, 881-889.
12. Vanderwolf, C.H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 26, 407-418.
13. Paz, R., Bauer, E.P., and Pare, D. (2008). Theta synchronizes the activity of medial prefrontal neurons during learning. Learn. Mem. 15, 524-531.
14. O'Neill, P.K., Gordon, J.A., and Sigurdsson, T. (2013). Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion. J. Neurosci. 33, 14211-14224.
15. Nerad, L., McNaughton, N. (2006). The septal EEG suggests a distributed organization of the pacemaker of hippocampal theta in the rat. Eur. J Neurosci. 24, 155-166.
16. Mattis, J., Brill, J., Evans, S., Lerner, T.N., Davidson, T.J., Hyun, M., Ramakrishnan, C., Deisseroth, K., and Huguenard, J.R. (2014). Frequency-dependent, cell type-divergent signaling in the hippocamposeptal projection. J. Neurosci. 34, 11769-11780.
17. Fedor, M., Berman, R.F., Muizelaar, J.P., and Lyeth, B.G. (2010). Hippocampal theta dysfunction after lateral fluid percussion injury. J. Neurotrauma 27, 1605-1615.
18. Lee, D.J., Gurkoff, G.G., Izadi, A., Berman, R.F., Ekstrom, A.D., Muizelaar, J.P., Lyeth, B.G., and Shahlaie, K. (2013). Medial septal nucleus theta frequency deep brain stimulation improves spatial working memory after traumatic brain injury. J. Neurotrauma 30:131-139.
19. Ennaceur, A., and Delacour, J. (1988). A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav. Brain Res. 31, 47-59.
20. Eacott, M.J., Easton, A., and Zinkivskay, A. (2005). Recollection in an episodic-like memory task in the rat. Learn. Mem. 12, 221-223.
21. Leutgeb, S., Leutgeb, J.K., Barnes, C.A., Moser, E.I., McNaughton, B.L., and Moser, M.B. (2005). Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309, 619-623.
22. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R.L., Hamm, R.J., Marmarou, A., Young, H.F., and Hayes, R.L. (1987). A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119.
23. McIntosh, T.K., Vink, R., Noble, L., Yamakami, I., Fernyak, S., Soares, H., and Faden, A.L. (1989). Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28, 233-244.
24. Addante, R.J., Watrous, A.J., Yonelinas, A.P., Ekstrom, A.D., and Ranganath, C. (2011). Prestimulus theta activity predicts correct source memory retrieval. Proc. Natl. Acad. Sci. U. S. A 108, 10702-10707.
25. Caplan, J.B., and Glaholt, M.G. (2007). The roles of EEG oscillations in learning relational information. Neuroimage 38, 604-616.
26. Caplan, J.B., Madsen, J.R., Raghavachari, S., and Kahana, M.J. (2001). Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. J. Neurophysiol. 86, 368-380.
27. Watrous, A.J., Tandon, N., Conner, C.R., Pieters, T., and Ekstrom, A.D. (2013). Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nat. Neurosci. 16, 349-356.
28. Delorme, A., and Makeig, S. (2004). EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9-21.
29. Vinck, M., van Wingerden, M., Womelsdorf, T., Fries, P., and Pennartz, C.M. (2010). The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization. Neuroimage 51, 112-122.
30. Lee, D.J., Gurkoff, G.G., Izadi, A., Berman, R.F., Ekstrom, A.D., Muizelaar, J.P., Lyeth, B.G., and Shahlaie, K. (2013). Medial septal nucleus theta frequency deep brain stimulation improves spatial working memory following traumatic brain injury. J. Neurotrauma 30, 131-139.
31. Winson, J. (1974). Patterns of hippocampal theta rhythm in the freely moving rat. Electroencephalogr. Clin. Neurophysiol. 36:291-301.
32. Nyhus, E., and Curran, T. (2010). Functional role of gamma and theta oscillations in episodic memory. Neurosci. Biobehav. Rev. 34, 1023-1035.
33. Gupta, A.S., van der Meer, M.A., Touretzky, D.S., and Redish, A.D. (2012). Segmentation of spatial experience by hippocampal theta sequences. Nat. Neurosci. 15, 1032-1039.
34. Sederberg, P.B., Kahana, M.J., Howard, M.W., Donner, E.J., and Madsen, J.R. (2003). Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci. 23, 10809-10814.
35. Jacobs, J., and Kahana, M.J. (2009). Neural representations of individual stimuli in humans revealed by gamma-band electrocorticographic activity. J. Neurosci. 29, 10203-10214.
36. Raghavachari, S., Kahana, M.J., Rizzuto, D.S., Caplan, J.B., Kirschen, M.P., Bourgeois, B., Madsen, J.R., and Lisman, J.E. (2001). Gating of human theta oscillations by a working memory task. J Neurosci.21: 3175-3183.
37. Lundqvist, M., Herman, P., and Lansner, A. (2011). Theta and gamma power increases and alpha/beta power decreases with memory load in an attractor network model. J. Cogn. Neurosci. 23:3008-3020.
38. Eakin, K., and Miller, J.P. (2012). Mild traumatic brain injury is associated with impaired hippocampal spatiotemporal representation in the absence of histological changes. J. Neurotrauma 29, 1180-1187.
39. Osaka, M., Osaka, N., Koyama, S., Okusa, T., and Kakigi, R. (1999). Individual differences in working memory and the peak alpha frequency shift on magnetoencephalography. Brain Res. Cogn. Brain. Res. 8, 365-368.
40. Buzsaki, G. (2002). Theta oscillations in the hippocampus. Neuron. 33, 325-340.
41. Giovannini, M.G., Rakovska, A., Benton, R.S., Pazzagli, M., Bianchi, L., and Pepeu, G. (2001). Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106, 43-53.
42. Vanderwolf, C.H. (1988). Cerebral activity and behavior: control by central cholinergic and serotonergic systems. Int. Rev. Neurobiol. 30, 225-340.
43. Geisler, C., Robbe, D., Zugaro, M., Sirota, A., and Buzsaki, G. (2007). Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. U. S. A.104, 8149-8154.
44. Jeewajee, A., Barry, C., O'Keefe, J., and Burgess, N. (2008). Grid cells and theta as oscillatory interference: electrophysiological data from freely moving rats. Hippocampus 18:1175-1185.
45. McFarland, W.L., Teitelbaum, H., and Hedges, E.K. (1975). Relationship between hippocampal theta activity and running speed in the rat. J. Comp. Physiol. Psychol. 88, 324-328.
46. Vertes, R.P., Albo, Z., and Viana Di Prisco, G. (2001). Thetarhythmically firing neurons in the anterior thalamus: implications for mnemonic functions of Papez's circuit. Neuroscience 104, 619-625.
47. Aggleton, J.P., O'Mara, S.M., Vann, S.D., Wright, N.F., Tsanov, M., and Erichsen, J.T. (2010). Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur. J Neurosci. 31, 2292-2307.
48. Hicks, R., Soares, H., Smith, D., and McIntosh, T. (1996). Temporal and spatial characterization of neuronal injury following lateral fluidpercussion brain injury in the rat. Acta Neuropathol. 91, 236-246.
49. Hallam, T.M., Floyd, C.L., Folkerts, M.M., Lee, L.L., Gong, Q.Z., Lyeth, B.G., Muizelaar, J.P., and Berman, R.F. (2004). Comparison of behavioral deficits and acute neuronal degeneration in rat lateral fluid percussion and weight-drop brain injury models. J. Neurotrauma 21, 521-539.
50. Cortez, S.C., McIntosh, T.K., and Noble, L.J. (1989). Experimental fluid percussion brain injury: vascular disruption and neuronal and glial alterations. Brain Res. 482, 271-282.
51. Conti, A.C., Raghupathi, R., Trojanowski, J.Q., and McIntosh, T.K. (1998). Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J. Neurosci. 18, 5663-5672.
52. Toth, Z., Hollrigel, G.S., Gorcs, T., and Soltesz, I. (1997). Instantaneous perturbation of dentate interneuronal networks by a pressure wave-transient delivered to the neocortex. J. Neurosci. 17, 8106-8117.
53. Lowenstein, D.H., Thomas, M.J., Smith, D.H., and McIntosh, T.K. (1992). Selective vulnerability of dentate hilar neurons following traumatic brain injury: a potential mechanistic link between head trauma and disorders of the hippocampus. J. Neurosci. 12, 4846-4853.
54. Hicks, R.R., Smith, D.H., Lowenstein, D.H., Saint Marie, R., and McIntosh, T.K. (1993). Mild experimental brain injury in the rat induces cognitive deficits associated with regional neuronal loss in the hippocampus. J. Neurotrauma 10, 405-414.
55. Bramlett, H.M., and Dietrich, W.D. (2002). Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol. 103, 607-614.
56. Dixon, C.E., Bao, J., Long, D.A., and Hayes, R.L. (1996). Reduced evoked release of acetylcholine in the rodent hippocampus following traumatic brain injury. Pharmacol. Biochem. Behav. 53, 679-686.
57. Dixon, C.E., Bao, J., Johnson, K.M., Yang, K., Whitson, J., Clifton, G.L., and Hayes, R.L. (1995). Basal and scopolamine-evoked release of hippocampal acetylcholine following traumatic brain injury in rats. Neurosci. Lett. 198, 111-114.
58. Dixon, C.E., Lyeth, B.G., Povlishock, J.T., Findling, R.L., Hamm, R.J., Marmarou, A., Young, H.F., and Hayes, R.L. (1987). A fluid percussion model of experimental brain injury in the rat. J. Neurosurg. 67, 110-119.
59. Gorman, L.K., Pang, K., Frick, K.M., Givens, B., and Olton, DS. (1994). Acetylcholine release in the hippocampus: effects of cholinergic and GABAergic compounds in the medial septal area. Neurosci. Lett. 166, 199-202.
60. Gorman, L.K., Fu, K., Hovda, D.A., Murray, M., and Traystman, R.J. (1996). Effects of traumatic brain injury on the cholinergic system in the rat. J. Neurotrauma 13, 457-463.
61. Lyeth, B.G., Jiang, J.Y., Delahunty, T.M., Phillips, L.L., and Hamm, R.J. (1994). Muscarinic cholinergic receptor binding in rat brain following traumatic brain injury. Brain Res. 640, 240-245.
62. Jiang, J.Y., Lyeth, B.G., Delahunty, T.M., Phillips, L.L., and Hamm R.J. (1994). Muscarinic cholinergic receptor binding in rat brain at 15 days following traumatic brain injury. Brain Res. 651, 123-128.
63. Verbois, S.L., Sullivan, P.G., Scheff, S.W., and Pauly, J.R. (2000). Traumatic brain injury reduces hippocampal alpha7 nicotinic cholinergic receptor binding. J. Neurotrauma 17, 1001-1011.
64. Verbois, S.L., Scheff, S.W., and Pauly, J.R. (2002). Time-dependent changes in rat brain cholinergic receptor expression after experimental brain injury. J. Neurotrauma 19, 1569-1585.
65. Reeves, T.M., Lyeth, B.G., Phillips, L.L., Hamm, R.J., and Povlishock, J.T. (1997). The effects of traumatic brain injury on inhibition in the hippocampus and dentate gyrus. Brain Res. 757, 119-132.
66. Gibson, C.J., Meyer, R.C., and Hamm, R.J. (2010). Traumatic brain injury and the effects of diazepam, diltiazem, and MK-801 on GABAA receptor subunit expression in rat hippocampus. J. Biomed. Sci. 17, 38.
67. Mtchedlishvili, Z., Lepsveridze, E., Xu, H., Kharlamov, E.A., Lu, B., and Kelly, K.M. (2010). Increase of GABAA receptor-mediated tonic inhibition in dentate granule cells after traumatic brain injury. Neurobiol. Dis. 38, 464-475.
68. Buzsaki, G., Czopf, J., Kondakor, I., and Kellenyi, L. (1986). Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current-source density analysis, effects of urethane and atropine. Brain Res. 365:125-137.
69. Watrous, A.J., Fried, I., and Ekstrom, A.D. (2011). Behavioral correlates of human hippocampal delta and theta oscillations during navigation. J. Neurophysiol. 105, 1747-1755.
70. Lipponen, A., Woldemichael, B.T., Gurevicius, K., and Tanila, H. (2012). Artificial theta stimulation impairs encoding of contextual fear memory. PLoS One 7, e48506.
71. Fell. J., Ludowig, E., Staresina, B.P., Wagner, T., Kranz, T., Elger, C.E., and Axmacher, N. (2011). Medial temporal theta/alpha power enhancement precedes successful memory encoding: evidence based on intracranial EEG. J. Neurosci. 31, 5392-5397.
72. Kleen, J.K., Wu, E.X., Holmes, G.L., Scott, R.C., and Lenck-Santini, P.P. (2011). Enhanced oscillatory activity in the hippocampalprefrontal network is related to short-term memory function after early-life seizures. J. Neurosci. 31, 15397-15406.
73. Rutishauser, U., Ross, I.B., Mamelak, A.N., and Schuman, E.M. (2010). Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903-907.